Ubiquitous heteroplasmy in Mytilus spp. resulting from disruption in doubly uniparental inheritance regulation

Species within the marine mussel Mytilus edulis complex (M. edulis, M. galloprovincialis, and M. trossulus) have an unusual form of mitochondrial DNA (mtDNA) inheritance commonly referred to as doubly uniparental inheritance (DUI). With DUI, all progeny inherit mtDNA maternally (F), while male progeny also inherit mtDNA paternally (M) through their father’s sperm. Therefore, females are normally homoplasmic for the F mtDNA, and males are heteroplasmic for the F and M mtDNA. In this study, we show that the regulation of DUI in populations of blue mussels in northern Japan is severely disrupted; consequently, the majority of individuals (89%) are heteroplasmic for M and F mtDNA. Disruption of DUI is primarily due to the failure of female embryos to exclude the father’s M mtDNA from their somatic and germinal tissues. High proportions of heteroplasmic females have only been reported in Japanese mussel populations thus far. We show that this disruption occurs in both parental species (M. trossulus and M. galloprovincialis) as well as hybrids and is independent of geographic location around Hokkaido, Japan. This finding differs from many previous studies, which have shown that disruption in DUI is confined to hybrid zones. In addition, some individuals were heteroplasmic for M or F mtDNA, indicating that DUI disruption is multigenerational. Triplasmic individuals were 3 times more often female and were mostly confined within the hybrid zones; however, a few individuals were found within M. galloprovincialis parental populations.